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Science 24 September 1993:
Vol. 261. no. 5129, pp. 1739 - 1744
DOI: 10.1126/science.8397445
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Articles

Science, Vol 261, Issue 5129, 1739-1744
Copyright © 1993 by American Association for the Advancement of Science

articles

A common nuclear signal transduction pathway activated by growth factor and cytokine receptors

HB Sadowski, K Shuai, JE Darnell Jr, and MZ Gilman

Cold Spring Harbor Laboratory, NY 11724.

Growth factors and cytokines act through cell surface receptors with different biochemical properties. Yet each type of receptor can elicit similar as well as distinct biological responses in target cells, suggesting that distinct classes of receptors activate common gene sets. Epidermal growth factor, interferon-gamma, and interleukin-6 all activated, through direct tyrosine phosphorylation, latent cytoplasmic transcription factors that recognized similar DNA elements. However, different ligands activated different patterns of factors with distinct DNA-binding specificities in the same and different cells. Thus, unrelated receptors may activate a common nuclear signal transduction pathway that, through differential use of latent cytoplasmic proteins, permits these receptors to regulate both common and unique sets of genes.


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T. L.-Y. Chang, A. Mosoian, R. Pine, M. E. Klotman, and J. P. Moore (2002)
J. Virol. 76, 569-581
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J. C. de Magalhaes, A. A. Andrade, P. N. G. Silva, L. P. Sousa, C. Ropert, P. C. P. Ferreira, E. G. Kroon, R. T. Gazzinelli, and C. A. Bonjardim (2001)
J. Biol. Chem. 276, 38353-38360
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GH Regulation of IGF-I and Suppressor of Cytokine Signaling Gene Expression in C2C12 Skeletal Muscle Cells.
C. L. Sadowski, T. T. Wheeler, L.-H. Wang, and H. B. Sadowski (2001)
Endocrinology 142, 3890-3900
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Abrogation of Transforming Growth Factor-{alpha}/Epidermal Growth Factor Receptor Autocrine Signaling by an RXR-selective Retinoid (LGD1069, Targretin) in Head and Neck Cancer Cell Lines.
J. I. Song, M. N. Lango, J. D. Hwang, S. D. Drenning, Q. Zeng, W. W. Lamph, and J. R. Grandis (2001)
Cancer Res. 61, 5919-5925
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Gelsolin as a Negative Prognostic Factor and Effector of Motility in erbB-2-positive Epidermal Growth Factor Receptor-positive Breast Cancers.
A. D. Thor, S. M. Edgerton, S. Liu, D. H. Moore II, and D. J. Kwiatkowski (2001)
Clin. Cancer Res. 7, 2415-2424
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Role of Signal Transducers and Activators of Transcription 1 and -3 in Inducible Regulation of the Human Angiotensinogen Gene by Interleukin-6.
C. T. Sherman and A. R. Brasier (2001)
Mol. Endocrinol. 15, 441-457
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A Novel Serine-dependent Proteolytic Activity Is Responsible for Truncated Signal Transducer and Activator of Transcription Proteins in Acute Myeloid Leukemia Blasts.
Z. Xia, R. R. Salzler, D. P. Kunz, M. R. Baer, L. Kazim, H. Baumann, and M. Wetzler (2001)
Cancer Res. 61, 1747-1753
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Constitutive activation of STAT3 is associated with the acquisition of an interleukin 6-independent phenotype by murine plasmacytomas and hybridomas.
R. Rawat, G. J. Rainey, C. D. Thompson, M. R. Frazier-Jessen, R. T. Brown, and R. P. Nordan (2000)
Blood 96, 3514-3521
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Regulation of STAT3 by Direct Binding to the Rac1 GTPase.
A. R. Simon, H. G. Vikis, S. Stewart, B. L. Fanburg, B. H. Cochran, and K.-L. Guan (2000)
Science 290, 144-147
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The Coiled-Coil Domain of Stat3 Is Essential for Its SH2 Domain-Mediated Receptor Binding and Subsequent Activation Induced by Epidermal Growth Factor and Interleukin-6.
T. Zhang, W. H. Kee, K. T. Seow, W. Fung, and X. Cao (2000)
Mol. Cell. Biol. 20, 7132-7139
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Loss of Interferon-{{gamma}} Inducibility of TAP1 and LMP2 in a Renal Cell Carcinoma Cell Line.
S. E. Dovhey, N. S. Ghosh, and K. L. Wright (2000)
Cancer Res. 60, 5789-5796
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The Role of Polypeptide Growth Factors in Human Carcinomas: New Targets for a Novel Pharmacological Approach.
R. E. Favoni and A. De Cupis (2000)
Pharmacol. Rev. 52, 179-206
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Constitutive activation of Stat3 signaling abrogates apoptosis in squamous cell carcinogenesis in vivo.
J. R. Grandis, S. D. Drenning, Q. Zeng, S. C. Watkins, M. F. Melhem, S. Endo, D. E. Johnson, L. Huang, Y. He, and J. D. Kim (2000)
PNAS 97, 4227-4232
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Transcriptional regulation of the MHC II gene DRA in untransformed human thyrocytes.
Z. Wu, P. A. Biro, R. Mirakian, F. Curcio, F. S. Ambesi-Impiombato, and G. F. Bottazzo (2000)
Int. Immunol. 12, 405-413
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Interleukin-4 Mediates Cell Growth Inhibition through Activation of Stat1.
T. L.-Y. Chang, X. Peng, and X.-Y. Fu (2000)
J. Biol. Chem. 275, 10212-10217
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L. H. Wang, X. Y. Yang, R. A. Kirken, J. H. Resau, and W. L. Farrar (2000)
Blood 95, 1249-1257
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LIF transduces contradictory signals on capillary outgrowth through induction of stat3 and (P41/43)MAP kinase.
H Paradis and R. Gendron (2000)
J. Cell Sci. 113, 4331-4339
   Abstract »    PDF »
How the Blood Talks to the Brain Parenchyma and the Paraventricular Nucleus of the Hypothalamus During Systemic Inflammatory and Infectious Stimuli.
S. Rivest, S. Lacroix, L. Vallières, S. Nadeau, J. Zhang, and N. Laflamme (2000)
Experimental Biology and Medicine 223, 22-38
   Abstract »    Full Text »
Platelet-derived Growth Factor Stimulation of Monocyte Chemoattractant Protein-1 Gene Expression Is Mediated by Transient Activation of the Phosphoinositide 3-Kinase Signal Transduction Pathway.
J. A. Alberta, K. R. Auger, D. Batt, P. Iannarelli, G. Hwang, H. L. Elliott, R. Duke, T. M. Roberts, and C. D. Stiles (1999)
J. Biol. Chem. 274, 31062-31067
   Abstract »    Full Text »    PDF »
Interacting Regions in Stat3 and c-Jun That Participate in Cooperative Transcriptional Activation.
X. Zhang, M. H. Wrzeszczynska, C. M. Horvath, and J. E. Darnell Jr. (1999)
Mol. Cell. Biol. 19, 7138-7146
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The Antiapoptotic Gene mcl-1 Is Up-Regulated by the Phosphatidylinositol 3-Kinase/Akt Signaling Pathway through a Transcription Factor Complex Containing CREB.
J.-M. Wang, J.-R. Chao, W. Chen, M.-L. Kuo, J. J.-Y. Yen, and H.-F. Yang-Yen (1999)
Mol. Cell. Biol. 19, 6195-6206
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Protein Kinase C delta Associates with and Phosphorylates Stat3 in an Interleukin-6-dependent Manner.
N. Jain, T. Zhang, W. H. Kee, W. Li, and X. Cao (1999)
J. Biol. Chem. 274, 24392-24400
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R.-H. Chen, M.-C. Chang, Y.-H. Su, Y.-T. Tsai, and M.-L. Kuo (1999)
J. Biol. Chem. 274, 23013-23019
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Oxidative Stress Triggers STAT3 Tyrosine Phosphorylation and Nuclear Translocation in Human Lymphocytes.
M. Carballo, M. Conde, R. El Bekay, J. Martin-Nieto, M. J. Camacho, J. Monteseirin, J. Conde, F. J. Bedoya, and F. Sobrino (1999)
J. Biol. Chem. 274, 17580-17586
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Negative Regulation by Protein Tyrosine Phosphatase of IFN-{gamma}-Dependent Expression of Inducible Nitric Oxide Synthase.
M. J. M. Diaz-Guerra, A. Castrillo, P. Martin-Sanz, and L. Bosca (1999)
J. Immunol. 162, 6776-6783
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Signaling in Human Osteoblasts by Extracellular Nucleotides. THEIR WEAK INDUCTION OF THE c-fos PROTO-ONCOGENE VIA Ca2+ MOBILIZATION IS STRONGLY POTENTIATED BY A PARATHYROID HORMONE/cAMP-DEPENDENT PROTEIN KINASE PATHWAY INDEPENDENTLY OF MITOGEN-ACTIVATED PROTEIN KINASE.
W. B. Bowler, C. J. Dixon, C. Halleux, R. Maier, G. Bilbe, W. D. Fraser, J. A. Gallagher, and R. A. Hipskind (1999)
J. Biol. Chem. 274, 14315-14324
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A Fatal Cytokine-Induced Systemic Inflammatory Response Reveals a Critical Role for NK Cells.
W. E. Carson, H. Yu, J. Dierksheide, K. Pfeffer, P. Bouchard, R. Clark, J. Durbin, A. S. Baldwin, J. Peschon, P. R. Johnson, et al. (1999)
J. Immunol. 162, 4943-4951
   Abstract »    Full Text »    PDF »
The STAT3-independent Signaling Pathway by Glycoprotein 130 in Hepatic Cells.
C.-f. Lai, J. Ripperger, Y. Wang, H. Kim, R. B. Hawley, and H. Baumann (1999)
J. Biol. Chem. 274, 7793-7802
   Abstract »    Full Text »    PDF »
Psoriatic keratinocytes show reduced IRF-1 and STAT-1{alpha} activation in response to {gamma}-IFN.
M. JACKSON, S. E. M. HOWIE, R. WELLER, E. SABIN, J. A. A. HUNTER, and R. C. McKENZIE (1999)
FASEB J 13, 495-502
   Abstract »    Full Text »
A Functional DNA Binding Domain Is Required for Growth Hormone-induced Nuclear Accumulation of Stat5B.
J. Herrington, L. Rui, G. Luo, L.-y. Yu-Lee, and C. Carter-Su (1999)
J. Biol. Chem. 274, 5138-5145
   Abstract »    Full Text »    PDF »
Identification of a STAT4 Binding Site in the Interleukin-12 Receptor Required for Signaling.
L. K. Naeger, J. McKinney, A. Salvekar, and T. Hoey (1999)
J. Biol. Chem. 274, 1875-1878
   Abstract »    Full Text »    PDF »
STAT5 Interaction with the T Cell Receptor Complex and Stimulation of T Cell Proliferation.
T. Welte, D. Leitenberg, B. N. Dittel, B. K. al-Ramadi, B. Xie, Y. E. Chin, C. A. Janeway Jr., A. L. Bothwell, K. Bottomly, and X. Fu (1999)
Science 283, 222-225
   Abstract »    Full Text »
Repression of Major Histocompatibility Complex Genes by a Human Trophoblast Ribonucleic Acid.
J. A. Peyman (1999)
Biol Reprod 60, 23-31
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Identification of a Novel Stat3 Recruitment and Activation Motif Within the Granulocyte Colony-Stimulating Factor Receptor.
A. Chakraborty, K. F. Dyer, M. Cascio, T. A. Mietzner, and D. J. Tweardy (1999)
Blood 93, 15-24
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Activation of the JAK-STAT pathway by reactive oxygen species.
A. R. Simon, U. Rai, B. L. Fanburg, and B. H. Cochran (1998)
Am J Physiol Cell Physiol 275, C1640-C1652
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Convergence of Progesterone with Growth Factor and Cytokine Signaling in Breast Cancer. PROGESTERONE RECEPTORS REGULATE SIGNAL TRANSDUCERS AND ACTIVATORS OF TRANSCRIPTION EXPRESSION AND ACTIVITY.
J. K. Richer, C. A. Lange, N. G. Manning, G. Owen, R. Powell, and K. B. Horwitz (1998)
J. Biol. Chem. 273, 31317-31326
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Inhibition of Stat1-mediated gene activation by PIAS1.
B. Liu, J. Liao, X. Rao, S. A. Kushner, C. D. Chung, D. D. Chang, and K. Shuai (1998)
PNAS 95, 10626-10631
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Synergistic Activation of MAP Kinase (ERK1/2) by Erythropoietin and Stem Cell Factor Is Essential for Expanded Erythropoiesis.
X. Sui, S. B. Krantz, M. You, and Z. Zhao (1998)
Blood 92, 1142-1149
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Characterization of the Role of the Human Granulocyte-Macrophage Colony-Stimulating Factor Receptor alpha  Subunit in the Activation of JAK2 and STAT5.
S. E. Doyle and J. C. Gasson (1998)
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Identification of a Membrane-associated Inhibitor(s) of Epidermal Growth Factor-induced Signal Transducer and Activator of Transcription Activation.
Y. Iwamoto, Y. E. Chin, X. Peng, and X.-Y. Fu (1998)
J. Biol. Chem. 273, 18198-18204
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Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3.
H. Niwa, T. Burdon, I. Chambers, and A. Smith (1998)
Genes & Dev. 12, 2048-2060
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TFII-I Enhances Activation of the c-fos Promoter through Interactions with Upstream Elements.
D.-W. Kim, V. Cheriyath, A. L. Roy, and B. H. Cochran (1998)
Mol. Cell. Biol. 18, 3310-3320
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Testicular Leukemia Inhibitory Factor (LIF) and LIF Receptor Mediate Phosphorylation of Signal Transducers and Activators of Transcription (STAT)-3 and STAT-1 and Induce c-fos Transcription and Activator Protein-1 Activation in Rat Sertoli But Not Germ Cells.
S. Jenab and P. L. Morris (1998)
Endocrinology 139, 1883-1890
   Abstract »    Full Text »    PDF »
Essential Role of Induced Nitric Oxide in the Initiation of the Inflammatory Response after Hemorrhagic Shock.
C. Hierholzer, B. Harbrecht, J. M. Menezes, J. Kane, J. MacMicking, C. F. Nathan, A. B. Peitzman, T. R. Billiar, and D. J. Tweardy (1998)
J. Exp. Med. 187, 917-928
   Abstract »    Full Text »    PDF »
Autoregulation of the Stat3 Gene through Cooperation with a cAMP-responsive Element-binding Protein.
M. Ichiba, K. Nakajima, Y. Yamanaka, N. Kiuchi, and T. Hirano (1998)
J. Biol. Chem. 273, 6132-6138
   Abstract »    Full Text »    PDF »
Protein Tyrosine Phosphatase 2 (SHP-2) Moderates Signaling by gp130 but Is Not Required for the Induction of Acute-Phase Plasma Protein Genes in Hepatic Cells.
H. Kim, T. S. Hawley, R. G. Hawley, and H. Baumann (1998)
Mol. Cell. Biol. 18, 1525-1533
   Abstract »    Full Text »
Oncostatin M Stimulates c-Fos to Bind a Transcriptionally Responsive AP-1 Element within the Tissue Inhibitor of Metalloproteinase-1 Promoter.
F. M. Botelho, D. R. Edwards, and C. D. Richards (1998)
J. Biol. Chem. 273, 5211-5218
   Abstract »    Full Text »    PDF »
Oncostatin M and the Interleukin-6 and Soluble Interleukin-6 Receptor Complex Regulate alpha 1-Antichymotrypsin Expression in Human Cortical Astrocytes.
T. Kordula, R. E. Rydel, E. F. Brigham, F. Horn, P. C. Heinrich, and J. Travis (1998)
J. Biol. Chem. 273, 4112-4118
   Abstract »    Full Text »    PDF »
Transmembrane Domain of gp130 Contributes to Intracellular Signal Transduction in Hepatic Cells.
H. Kim and H. Baumann (1997)
J. Biol. Chem. 272, 30741-30747
   Abstract »    Full Text »    PDF »
Specific Inhibition of Stat3 Signal Transduction by PIAS3.
C. D. Chung, J. Liao, B. Liu, X. Rao, P. Jay, P. Berta, and K. Shuai (1997)
Science 278, 1803-1805
   Abstract »    Full Text »
Leukemia Inhibitory Factor, a Potent Cardiac Hypertrophic Cytokine, Activates the JAK/STAT Pathway in Rat Cardiomyocytes.
H. Kodama, K. Fukuda, J. Pan, S. Makino, A. Baba, S. Hori, and S. Ogawa (1997)
Circ. Res. 81, 656-663
   Abstract »    Full Text »
Role of Angiotensin II in Activation of the JAK/STAT Pathway Induced by Acute Pressure Overload in the Rat Heart.
J. Pan, K. Fukuda, H. Kodama, S. Makino, T. Takahashi, M. Sano, S. Hori, and S. Ogawa (1997)
Circ. Res. 81, 611-617
   Abstract »    Full Text »
Signal Transducer and Activator of Transcription-3 Serine Phosphorylation by Insulin Is Mediated by a Ras/Raf/MEK-Dependent Pathway.
B. P. Ceresa, C. M. Horvath, and J. E. Pessin (1997)
Endocrinology 138, 4131-4137
   Abstract »    Full Text »    PDF »
A multifunctional DNA-binding protein that promotes the formation of serum response factor/homeodomain complexes: identity to TFII-I.
D. A. Grueneberg, R. W. Henry, A. Brauer, C. D. Novina, V. Cheriyath, A. L. Roy, and M. Gilman (1997)
Genes & Dev. 11, 2482-2493
   Abstract »    Full Text »    PDF »
Constitutive and impaired signaling of leptin receptors containing the Gln right-arrow Pro extracellular domain fatty mutation.
D. W.W. Y. Wang, S. C. Chua Jr., J. P. Morgenstern, R. L. Leibel, H. Baumann, and L. A. Tartaglia (1997)
PNAS 94, 10657-10662
   Abstract »    Full Text »    PDF »
Leukemia Inhibitory Factor-dependent Transcriptional Activation in Embryonic Stem Cells.
H. Boeuf, C. Hauss, F. D. Graeve, N. Baran, and C. Kedinger (1997)
J. Cell Biol. 138, 1207-1217
   Abstract »    Full Text »    PDF »
Positive Effects of SH2 Domain-containing Tyrosine Phosphatase SHP-1 on Epidermal Growth Factor- and Interferon-gamma -stimulated Activation of STAT Transcription Factors in HeLa Cells.
M. You and Z. Zhao (1997)
J. Biol. Chem. 272, 23376-23381
   Abstract »    Full Text »    PDF »
Calcium Controls Gene Expression via Three Distinct Pathways That Can Function Independently of the Ras/Mitogen-Activated Protein Kinases (ERKs) Signaling Cascade.
C. M. Johnson, C. S. Hill, S. Chawla, R. Treisman, and H. Bading (1997)
J. Neurosci. 17, 6189-6202
   Abstract »    Full Text »    PDF »
New Advances in Interferon Therapy of Cancer.
S. Wadler and E. L. Schwartz (1997)
Oncologist 2, 254-267
   Abstract »    Full Text »    PDF »
Alternative Signaling Mechanism of Leukemia Inhibitory Factor Responsiveness in a Differentiating Embryonal Carcinoma Cell.
T. Takeda, H. Kurachi, T. Yamamoto, H. Homma, K. Adachi, K. Morishige, A. Miyake, and Y. Murata (1997)
Endocrinology 138, 2689-2696
   Abstract »    Full Text »    PDF »
Transcriptional Regulation of Sertoli Cell Immediate Early Genes by Interleukin-6 and Interferon-{gamma} Is Mediated through Phosphorylation of STAT-3 and STAT-1 Proteins.
S. Jenab and P. L. Morris (1997)
Endocrinology 138, 2740-2746
   Abstract »    Full Text »    PDF »


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